Demography of the understory herb Heliconia acuminata (Heliconiaceae) in an experimentally fragmented tropical landscape.

Habitat fragmentation remains a major focus of research by ecologists decades after being put forward as a threat to the integrity of ecosystems. While studies have documented myriad biotic changes in fragmented landscapes, including the local extinction of species from fragments, the demographic mechanisms underlying these extinctions are rarely known. However, many of them-especially in lowland tropical forests-are thought to be driven by one of two mechanisms: (1) reduced recruitment in fragments resulting from changes in the diversity or abundance of pollinators and seed dispersers or (2) increased rates of individual mortality in fragments due to dramatically altered abiotic conditions, especially near fragment edges. Unfortunately, there have been few tests of these potential mechanisms due to the paucity of long-term and comprehensive demographic data collected in both forest fragments and continuous forest sites. Here we report 11 years (1998-2009) of demographic data from populations of the Amazonian understory herb Heliconia acuminata (LC Rich.) found at Brazil's Biological Dynamics of Forest Fragments Project (BDFFP). The data set comprises >66,000 plant × year records of 8586 plants, including 3464 seedlings established after the first census. Seven populations were in experimentally isolated fragments (one in each of four 1-ha fragments and one in each of three 10-ha fragments), with the remaining six populations in continuous forest. Each population was in a 50 × 100 m permanent plot, with the distance between plots ranging from 500 m to 60 km. The plants in each plot were censused annually, at which time we recorded, identified, marked, and measured new seedlings, identified any previously marked plants that died, and recorded the size of surviving individuals. Each plot was also surveyed four to five times during the flowering season to identify reproductive plants and record the number of inflorescences each produced. These data have been used to investigate topics ranging from the way fragmentation-related reductions in germination influence population dynamics to statistical methods for analyzing reproductive rates. This breadth of prior use reflects the value of these data to future researchers. In addition to analyses of plant responses to habitat fragmentation, these data can be used to address fundamental questions in plant demography and the evolutionary ecology of tropical plants and to develop and test demographic models and tools. Though we welcome opportunities to collaborate with interested users, there are no restrictions on the use of this data set. However, we do request that those using the data for teaching or research purposes inform us of how they are doing so and cite this paper and the data archive when appropriate. Any publication using the data must also include a BDFFP Technical Series Number in the Acknowledgments. Authors can request this series number upon the acceptance of their article by contacting the BDFFP's Scientific Coordinator or E. M. Bruna.

Landscape experiments unlock relationships among habitat loss, fragmentation, and patch-size effects.

Habitat loss is often considered the greatest near-term threat to biodiversity, while the impact of habitat fragmentation remains intensely debated. A key issue of this debate centers on the problem of scale-landscape or patch-at which to assess the consequences of fragmentation. Yet patterns are often confounded across scales, and experimental designs that could solve this scaling problem remain scarce. We conducted two field experiments in 30 experimental landscapes in which we manipulated habitat loss, fragmentation, and patch size for a community of four insect herbivores that specialize on the cactus Opuntia. In the first experiment, we destroyed 2088 Opuntia patches in either aggregated or random patterns and compared the relative effects of landscape-scale loss and fragmentation to those of local patch size on species occurrence. This experiment focused on manipulating the relative separation of remaining patches, where we hypothesized that aggregated loss would disrupt dispersal more than random loss, leading to lower occurrence. In the second experiment, we destroyed 759 Opuntia patches to generate landscapes that varied in patch number and size for a given amount of habitat loss and assessed species occurrence. This experiment focused on manipulating the subdivision of remaining habitat, where we hypothesized that an increase in the number of patches for a given amount of loss would lead to negative effects on occurrence. For both, we expected that occurrence would increase with patch size. We find strong evidence for landscape-scale effects of habitat fragmentation, with aggregated loss and a larger number of patches for a given amount of habitat loss leading to a lower frequency of patches occupied in landscapes. In both experiments, occurrence increased with patch size, yet interactions of patch size and landscape-scale loss and fragmentation drove species occurrence in patches. Importantly, the direction of effects were consistent across scales and effects of patch size were sufficient to predict the effects of habitat loss and fragmentation across entire landscapes. Our experimental results suggest that changes at both the patch and landscape scales can impact populations, but that a long-standing pattern-the patch-size effect-captures much of the key variation shaping patterns of species occurrence.

Integrating tropical research into biology education is urgently needed.

Understanding tropical biology is important for solving complex problems such as climate change, biodiversity loss, and zoonotic pandemics, but biology curricula view research mostly via a temperate-zone lens. Integrating tropical research into biology education is urgently needed to tackle these issues.

Delayed effects of climate on vital rates lead to demographic divergence in Amazonian forest fragments.

Deforestation often results in landscapes where remaining forest habitat is highly fragmented, with remnants of different sizes embedded in an often highly contrasting matrix. Local extinction of species from individual fragments is common, but the demographic mechanisms underlying these extinctions are poorly understood. It is often hypothesized that altered environmental conditions in fragments drive declines in reproduction, recruitment, or survivorship. The Amazon basin, in addition to experiencing continuing fragmentation, is experiencing climate change-related increases in the frequency and intensity of droughts and unusually wet periods. Whether plant populations in tropical forest fragments are particularly susceptible to extremes in precipitation remains unclear. Most studies of plants in fragments are relatively short (1-6 years), focus on a single life-history stage, and often do not compare to populations in continuous forest. Even fewer studies consider delayed effects of climate on demographic vital rates despite the importance of delayed effects in studies that consider them. Using a decade of demographic and climate data from an experimentally fragmented landscape in the Central Amazon, we assess the effects of climate on populations of an understory herb (Heliconia acuminata, Heliconiaceae). We used distributed lag nonlinear models to understand the delayed effects of climate (measured as standardized precipitation evapotranspiration index, SPEI) on survival, growth, and flowering. We detected delayed effects of climate up to 36 months. Extremes in SPEI in the previous year reduced survival, drought in the wet season 8-11 months prior to the February census increased growth, and drought two dry seasons prior increased flowering probability. Effects of extremes in precipitation on survival and growth were more pronounced in forest fragments compared to continuous forest. The complex delayed effects of climate and habitat fragmentation in our study point to the importance of long-term demography experiments in understanding the effects of anthropogenic change on plant populations.

Advancing an interdisciplinary framework to study seed dispersal ecology.

Although dispersal is generally viewed as a crucial determinant for the fitness of any organism, our understanding of its role in the persistence and spread of plant populations remains incomplete. Generalizing and predicting dispersal processes are challenging due to context dependence of seed dispersal, environmental heterogeneity and interdependent processes occurring over multiple spatial and temporal scales. Current population models often use simple phenomenological descriptions of dispersal processes, limiting their ability to examine the role of population persistence and spread, especially under global change. To move seed dispersal ecology forward, we need to evaluate the impact of any single seed dispersal event within the full spatial and temporal context of a plant's life history and environmental variability that ultimately influences a population's ability to persist and spread. In this perspective, we provide guidance on integrating empirical and theoretical approaches that account for the context dependency of seed dispersal to improve our ability to generalize and predict the consequences of dispersal, and its anthropogenic alteration, across systems. We synthesize suitable theoretical frameworks for this work and discuss concepts, approaches and available data from diverse subdisciplines to help operationalize concepts, highlight recent breakthroughs across research areas and discuss ongoing challenges and open questions. We address knowledge gaps in the movement ecology of seeds and the integration of dispersal and demography that could benefit from such a synthesis. With an interdisciplinary perspective, we will be able to better understand how global change will impact seed dispersal processes, and potential cascading effects on plant population persistence, spread and biodiversity.

Towards a unified framework for connectivity that disentangles movement and mortality in space and time.

Predicting connectivity, or how landscapes alter movement, is essential for understanding the scope for species persistence with environmental change. Although it is well known that movement is risky, connectivity modelling often conflates behavioural responses to the matrix through which animals disperse with mortality risk. We derive new connectivity models using random walk theory, based on the concept of spatial absorbing Markov chains. These models decompose the role of matrix on movement behaviour and mortality risk, can incorporate species distribution to predict the amount of flow, and provide both short- and long-term analytical solutions for multiple connectivity metrics. We validate the framework using data on movement of an insect herbivore in 15 experimental landscapes. Our results demonstrate that disentangling the roles of movement behaviour and mortality risk is fundamental to accurately interpreting landscape connectivity, and that spatial absorbing Markov chains provide a generalisable and powerful framework with which to do so.

Employing plant functional groups to advance seed dispersal ecology and conservation.

Seed dispersal enables plants to reach hospitable germination sites and escape natural enemies. Understanding when and how much seed dispersal matters to plant fitness is critical for understanding plant population and community dynamics. At the same time, the complexity of factors that determine if a seed will be successfully dispersed and subsequently develop into a reproductive plant is daunting. Quantifying all factors that may influence seed dispersal effectiveness for any potential seed-vector relationship would require an unrealistically large amount of time, materials and financial resources. On the other hand, being able to make dispersal predictions is critical for predicting whether single species and entire ecosystems will be resilient to global change. Building on current frameworks, we here posit that seed dispersal ecology should adopt plant functional groups as analytical units to reduce this complexity to manageable levels. Functional groups can be used to distinguish, for their constituent species, whether it matters (i) if seeds are dispersed, (ii) into what context they are dispersed and (iii) what vectors disperse them. To avoid overgeneralization, we propose that the utility of these functional groups may be assessed by generating predictions based on the groups and then testing those predictions against species-specific data. We suggest that data collection and analysis can then be guided by robust functional group definitions. Generalizing across similar species in this way could help us to better understand the population and community dynamics of plants and tackle the complexity of seed dispersal as well as its disruption.

Statistical modeling of patterns in annual reproductive rates.

Reproduction by individuals is typically recorded as count data (e.g., number of fledglings from a nest or inflorescences on a plant) and commonly modeled using Poisson or negative binomial distributions, which assume that variance is greater than or equal to the mean. However, distributions of reproductive effort are often underdispersed (i.e., variance < mean). When used in hypothesis tests, models that ignore underdispersion will be overly conservative and may fail to detect significant patterns. Here we show that generalized Poisson (GP) and Conway-Maxwell-Poisson (CMP) distributions are better choices for modeling reproductive effort because they can handle both overdispersion and underdispersion; we provide examples of how ecologists can use GP and CMP distributions in generalized linear models (GLMs) and generalized linear mixed models (GLMMs) to quantify patterns in reproduction. Using a new R package, glmmTMB, we construct GLMMs to investigate how rainfall and population density influence the number of fledglings in the warbler Oreothlypis celata and how flowering rate of Heliconia acuminata differs between fragmented and continuous forest. We also demonstrate how to deal with zero-inflation, which occurs when there are more zeros than expected in the distribution, e.g., due to complete reproductive failure by some individuals.

Do an ecosystem engineer and environmental gradient act independently or in concert to shape juvenile plant communities? Tests with the leaf-cutter ant Atta laevigata in a Neotropical savanna.

BACKGROUND: Ecosystem engineers are species that transform habitats in ways that influence other species.While the impacts of many engineers have been well described, our understanding of how their impact varies along environmental gradients remains limited. Although disentangling the effects of gradients and engineers on biodiversity is complicated-the gradients themselves can be altered by engineers-doing so is necessary to advance conceptual and mathematical models of ecosystem engineering. We used leaf-cutter ants (Atta spp.) to investigate the relative influence of gradients and environmental engineers on the abundance and species richness of woody plants. METHODS: We conducted our research in South America's Cerrado. With a survey of plant recruits along a canopy cover gradient, and data on environmental conditions that influence plant recruitment, we fit statistical models that addressed the following questions: (1) Does A. laevigata modify the gradient in canopy cover found in our Cerrado site? (2) Do environmental conditions that influence woody plant establishment in the Cerrado vary with canopy cover or proximity to A. laevigata nests? (3) Do A. laevigata and canopy cover act independently or in concert to influence recruit abundance and species richness? RESULTS: We found that environmental conditions previously shown to influence plant establishment in the Cerrado varied in concert with canopy cover, but that ants are not modifying the cover gradient or cover over nests. However, ants are modifying other local environmental conditions, and the magnitude and spatial extent of these changes are consistent across the gradient. In contrast to prior studies, we found that ant-related factors (e.g., proximity to nests, ant changes in surface conditions), rather than canopy cover, had the strongest effect on the abundance of plant recruits. However, the diversity of plants was influenced by both the engineer and the canopy cover gradient. DISCUSSION: Atta laevigata in the Cerrado modify local conditions in ways that have strong but spatially restricted consequences for plant communities. We hypothesize that ants indirectly reduce seedling establishment by clearing litter and reducing soil moisture, which leads to seed and seedling desiccation. Altering soil nutrients could also reduce juvenile growth and survivorship; if so these indirect negative effects of engineering could exacerbate their direct effects of harvesting plants. The effects of Atta appear restricted to nest mounds, but they could be long-lasting because mounds persist long after a colony has died or migrated. Our results support the hypothesis that leaf-cutter ants play a dominant role in Cerrado plant demography. We suggest the ecological and economic footprint of these engineers may increase dramatically in coming decades due to the transformation of the Cerrado by human activities.

A persistent lack of international representation on editorial boards in environmental biology.

The scholars comprising journal editorial boards play a critical role in defining the trajectory of knowledge in their field. Nevertheless, studies of editorial board composition remain rare, especially those focusing on journals publishing research in the increasingly globalized fields of science, technology, engineering, and math (STEM). Using metrics for quantifying the diversity of ecological communities, we quantified international representation on the 1985-2014 editorial boards of 24 environmental biology journals. Over the course of 3 decades, there were 3,827 unique scientists based in 70 countries who served as editors. The size of the editorial community increased over time-the number of editors serving in 2014 was 4-fold greater than in 1985-as did the number of countries in which editors were based. Nevertheless, editors based outside the "Global North" (the group of economically developed countries with high per capita gross domestic product [GDP] that collectively concentrate most global wealth) were extremely rare. Furthermore, 67.18% of all editors were based in either the United States or the United Kingdom. Consequently, geographic diversity-already low in 1985-remained unchanged through 2014. We argue that this limited geographic diversity can detrimentally affect the creativity of scholarship published in journals, the progress and direction of research, the composition of the STEM workforce, and the development of science in Latin America, Africa, the Middle East, and much of Asia (i.e., the "Global South").

A whole-plant perspective reveals unexpected impacts of above- and belowground herbivores on plant growth and defense.

Trade-offs between plant growth and defense are central to theoretical frameworks used to study the ecology and evolution of plant defense against herbivores. However, these frameworks, as well as the experiments designed to test them, rarely include belowground herbivores. We experimentally challenged seedlings of the tropical shrub Solanum lycocarpum (Solanaceae) with either aboveground foliar herbivores (Spodoptera caterpillars) or belowground root herbivores (the nematode Meloidogyne incognita) and measured the resulting changes in plant growth rates, biomass allocation, and the concentration of defensive terpenoids in roots and leaves. We found that plants that suffered aboveground herbivory responded with aboveground growth but belowground defense. Similarly, belowground herbivory resulted in root growth but elevated defenses of leaves. These results underscore the importance of belowground plant-herbivore interactions, and suggest that, in contrast to theoretical predictions, plants can simultaneously invest in both growth and defense. Finally, they emphasize the need for a "whole-plant" perspective in theoretical and empirical evaluations of plant-herbivore interactions.

Is There a Temperate Bias in Our Understanding of How Climate Change Will Alter Plant-Herbivore Interactions? A Meta-analysis of Experimental Studies.

Climate change can drive major shifts in community composition and interactions between resident species. However, the magnitude of these changes depends on the type of interactions and the biome in which they take place. We review the existing conceptual framework for how climate change will influence tropical plant-herbivore interactions and formalize a similar framework for the temperate zone. We then conduct the first biome-specific tests of how plant-herbivore interactions change in response to climate-driven changes in temperature, precipitation, ambient CO2, and ozone. We used quantitative meta-analysis to compare predicted and observed changes in experimental studies. Empirical studies were heavily biased toward temperate systems, so testing predicted changes in tropical plant-herbivore interactions was virtually impossible. Furthermore, most studies investigated the effects of CO2 with limited plant and herbivore species. Irrespective of location, most studies manipulated only one climate change factor despite the fact that different factors can act in synergy to alter responses of plants and herbivores. Finally, studies of belowground plant-herbivore interactions were also rare; those conducted suggest that climate change could have major effects on belowground subsystems. Our results suggest that there is a disconnection between the growing literature proposing how climate change will influence plant-herbivore interactions and the studies testing these predictions. General conclusions will also be hampered without better integration of above- and belowground systems, assessing the effects of multiple climate change factors simultaneously, and using greater diversity of species in experiments.

The scientific impact of nations: journal placement and citation performance.

International collaboration is becoming increasingly important for the advancement of science. To gain a more precise understanding of how factors such as international collaboration influence publication success, we divide publication success into two categories: journal placement and citation performance. Analyzing all papers published between 1996 and 2012 in eight disciplines, we find that those with more countries in their affiliations performed better in both categories. Furthermore, specific countries vary in their effects both individually and in combination. Finally, we look at the relationship between national output (in papers published) and input (in citations received) over the 17 years, expanding upon prior depictions by also plotting an expected proportion of citations based on Journal Placement. Discrepancies between this expectation and the realized proportion of citations illuminate trends in performance, such as the decline of the Global North in response to rapidly developing countries, especially China. Yet, most countries' show little to no discrepancy, meaning that, in most cases, citation proportion can be predicted by Journal Placement alone. This reveals an extreme asymmetry between the opinions of a few reviewers and the degree to which paper acceptance and citation rates influence career advancement.

Women are underrepresented on the editorial boards of journals in environmental biology and natural resource management.

Despite women earning similar numbers of graduate degrees as men in STEM disciplines, they are underrepresented in upper level positions in both academia and industry. Editorial board memberships are an important example of such positions; membership is both a professional honor in recognition of achievement and an opportunity for professional advancement. We surveyed 10 highly regarded journals in environmental biology, natural resource management, and plant sciences to quantify the number of women on their editorial boards and in positions of editorial leadership (i.e., Associate Editors and Editors-in-Chief) from 1985 to 2013. We found that during this time period only 16% of subject editors were women, with more pronounced disparities in positions of editorial leadership. Although the trend was towards improvement over time, there was surprising variation between journals, including those with similar disciplinary foci. While demographic changes in academia may reduce these disparities over time, we argue journals should proactively strive for gender parity on their editorial boards. This will both increase the number of women afforded the opportunities and benefits that accompany board membership and increase the number of role models and potential mentors for early-career scientists and students.

Low plant density enhances gene dispersal in the Amazonian understory herb Heliconia acuminata.

In theory, conservation genetics predicts that forest fragmentation will reduce gene dispersal, but in practice, genetic and ecological processes are also dependent on other population characteristics. We used Bayesian genetic analyses to characterize parentage and propagule dispersal in Heliconia acuminata L. C. Richard (Heliconiaceae), a common Amazonian understory plant that is pollinated and dispersed by birds. We studied these processes in two continuous forest sites and three 1-ha fragments in Brazil's Biological Dynamics of Forest Fragments Project. These sites showed variation in the density of H. acuminata. Ten microsatellite markers were used to genotype flowering adults and seedling recruits and to quantify realized pollen and seed dispersal distances, immigration of propagules from outside populations, and reproductive dominance among parents. We tested whether gene dispersal is more dependent on fragmentation or density of reproductive plants. Low plant densities were associated with elevated immigration rates and greater propagule dispersal distances. Reproductive dominance among inside-plot parents was higher for low-density than for high-density populations. Elevated local flower and fruit availability is probably leading to spatially more proximal bird foraging and propagule dispersal in areas with high density of reproductive plants. Nevertheless, genetic diversity, inbreeding coefficients and fine-scale spatial genetic structure were similar across populations, despite differences in gene dispersal. This result may indicate that the opposing processes of longer dispersal events in low-density populations vs. higher diversity of contributing parents in high-density populations balance the resulting genetic outcomes and prevent genetic erosion in small populations and fragments.